Research Article Persistent Primitive Olfactory Artery in ...primitive olfactory artery (PO A)...

Hindawi Publishing CorporationBioMed Research InternationalVolume 2013, Article ID 903460, 7 pageshttp://dx.doi.org/10.1155/2013/903460

Research ArticlePersistent Primitive Olfactory Artery in Serbian Population

Ljiljana VasoviT,1 Milena TrandafiloviT,2 Slobodan VlajkoviT,1

Ivan JovanoviT,1 and SlaZana UgrenoviT1

1 Department of Anatomy, Faculty of Medicine, University of Nis, Boulevard Dr. Zoran Ðinđic 81, 18000 Nis, Serbia2 Center for Biomedical Researches, Faculty of Medicine, University of Nis, Boulevard Dr. Zoran Ðinđic 81, 18000 Nis, Serbia

Correspondence should be addressed to Ljiljana Vasovic; [email protected]

Received 11 April 2013; Accepted 17 June 2013

Academic Editor: Hongjuan Liu

Copyright © 2013 Ljiljana Vasovic et al.This is an open access article distributed under the Creative Commons Attribution License,which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

The continuation of the cranial branch of the primitive internal carotid artery is called the primitive olfactory artery (POℓA). Ittakes this name according to the fact that it is mainly concerned with supplying the developing nasal region. We reported twonew cases of the persistent POℓA (PPOℓA) in Serbian population after retrospective analysis of digital images of 200 fetal and 269adult cases. This PPOℓA originated from the precommunicating part (A1) of the right anterior cerebral artery, coursed along theolfactory tract, and turned on the medial cerebral hemisphere in both male adults. Some vascular variations (fenestration of the A1and the median artery of the corpus callosum) were associated with this persistent vessel. According to the fact that we did not findaneurysm in our previous and two recent cases, we are of the opinion that PPOℓA is usually asymptomatic in Serbian population.

1. Introduction

During embryonic development of the vascular system, theprimitive olfactory artery (POℓA) represents a continuationof the cranial branch of the primitive internal carotid artery(ICA) [1]. It may be presumed that a fenestration of theanterior cerebral artery (ACA) is the remnant of the embry-onal plexiform anastomosis between the ACA and the POℓA[2, 3]. Some authors noted that POℓA normally regresses tothe remnant—the recurrent artery of Heubner (RAH) [4, 5].Other authors supported this claim by the evidence of anaplasia of the RAH [6–8] and/or the anterior communicatingartery [6, 9].

A persistence of the POℓA (PPOℓA) is very rare accord-ing to the fact that its incidence was noted in 0.14% [10] to0.29% [11] of cases.

Morphologically, the PPOℓA usually courses anterome-dially along the ipsilateral olfactory tract, and after a turn, itsupplies theACA territory [4]. Pathoanatomically, a relativelyfrequent location of an aneurysm on the hairpin bend of thePPOℓA emphasizes the importance of hemodynamic stressin this persistent primitive vessel [7, 12, 13].

Reports of single cases or retrospective studies aboutspecial and/or general features of the PPOℓA came usually

from Japan [5–10, 12–17] and Korea [11, 18, 19], although therewere case reports fromUK [20], Taiwan [21], and Serbia [22].

Previous incidental finding of the PPOℓA in one adultcadaver [22], and the description of fenestration of theprecommunicating part (A1) of the ACA [3] and/or RAH infetuses [23], inspired us to amore detailed investigation of thePOℓA persistence in Serbian population.

2. Materials and Methods

We did a retrospective analysis of digital images of brainvessels of 200 fetal and 269 adult cadavers, dissected at theDepartment of Anatomy and Institute of Forensic Medicinein Nis, respectively.

2.1. Fetal Cadavers. Fetuses of both genders, from 9 to 32weeks of gestation, were a part of the collection of ourDepartment of Anatomy, and they were used in the prepara-tion of doctoral thesis [24]. All fetuses were obtained legallyfrom the Clinic of Gynecology and Obstetrics in Nis. TheCouncil for Postgraduate Study of the Faculty of Medicinein Nis gave permission to investigate the fetal material. Thearteries of fetuses were injected with Micropaque or latex

2 BioMed Research International

through the left cardiac ventricle or through the commoncarotid artery. All fetuses were fixed in 10% formalin for2 weeks. Fetal brains were removed and kept in individualcalvarias. The measurements were performed by means ofan ocular micrometer mounted on an operating microscope(Olympus).

2.2. Adult Cadavers. The dissected brains originated fromcadavers of both genders, different ages (from the neonate to95 years), and different causes of death in the period between2006 and 2013. Investigation of these cases was in accordancewith the rules of the internal Ethics Committee (no. 01-9068-4) of our Faculty of Medicine. Morphological features ofbrain arteries (caliber, possible vessel’s abnormalities) wereobserved by using a magnifying glass and recorded on afilm. Measurement of the external diameter of arteries wasperformed by ImageJ (http://rsb.info.nih.gov/ij/index.html).

3. Results and Discussion

3.1. Results. We discovered two new cases of the PPOℓA inadults. The first case of the PPOℓA was found in a malecadaver, aged 58 and autopsied due to cardiac arrest; anothercasewas found in amale, aged 61, whodied due to polytraumaat the Orthopedic Clinic.

(1) Case I. The PPOℓA had a common origin with theRAH from the A1 of the right ACA at the level ofthe proximal part of the fenestration (Figure 1(a)). Itsbeginning was about 7mm away from ICA bifurca-tion.The caliber of the right A1 was 2.03mm, whereasthe caliber of the PPOℓA was 1.41mm. The latterfollowed the olfactory tract in the first part of itscourse, and after that, it turned and passed on themedial telencephalic surface. However, we did notphotograph its termination. In addition, the medianartery of the corpus callosum was also presented(Figure 1(b)).

(2) Case II. The PPOℓA was a branch of the right A1(Figure 2(a)).The beginning of the PPOℓAwas about6mm away from ICA bifurcation. The caliber ofthe right A1 was 2.50mm, whereas caliber of thePPOℓAwas 1.40mm.The latter followed the olfactorytract in the first part of its course, and after that,it passed similar to the callosomarginal artery; abihemispheric branch was also evidenced at the levelof its termination (Figure 2(b)). Ipsilaterally, the RAHoriginated from the PPOℓA; it was duplicated at thebeginning. Atherosclerotic plaques were significantlypresent at the cerebral arteries, especially along mainbrain arteries.

(3) Comparison of PPOℓAs in the Literature. Generaland special data about PPOℓAs in our and otherpopulations are presented in Table 1.

3.2. Discussion. Firstly, we noted some data and disagree-ments in the literature about the POℓAorigin [1, 6, 25], POℓArudiments [1] or a lack of embryologic explanation of A1

variable side branches [15, 26], as well as an origin [20] ortermination [8, 15] of the PPOℓA.

Moffat [1] described that POℓAhas a similar developmentin the rat’s and human embryos up to an 18mm stage. Duringthe development of vascular system in a 3.7mm embryo, thecontinuation of the dorsal aorta forms the primitive ICA [1],except for its first segment which was formed by the primitivethird aortic arch [6]. At the level of the forebrain the ICAgives the primitivemaxillary artery, and then ICAdivides intothe cranial and caudal branches. In embryos of 4 to 5.7mm(28–30 days), the cranial branch constitutes the primitiveolfactory artery (POℓA), which branches off the anteriorchoroidal and middle cerebral arteries [6]. According todata from the paper by Horie et al. [13], the definitiveACA extends superiorly between the cerebral hemispheres,associated with regression of the POℓA untill the 7th weekof gestation. According to the picture of human embryo inthe paper by Katayama et al. [14], the POℓA retains its originfrom the A1 to the 9mm embryonic stage. Komiyama [25]and Okahara et al. [6] stressed that the POℓA terminatesin the nasal fossa, and “secondary artery” constitutes themedial olfactory artery, which supplies the olfactory bulb.This medial olfactory artery becomes the ACA proper in an11.5 to 18mmembryo, while the terminal portion of the POℓAusually regresses. Kim et al. [27] noted the existence of theplexiformanastomosis between theACAand thePOℓA in theillustration of a 14mm embryo. Lateral olfactory branches ofthe POℓA include the RAH, anterior choroidal, lateral striate,and middle cerebral arteries. Moffat [1] noted that the POℓAin a 24mmhuman embryo forms an inconstant striate branchof the ACA.

Okahara et al. [6] noted that the PPOℓA arises only fromthe A1 part, as in cases described by Moffat [20] and Horieet al. [13], as well as in recent cases. In addition, we couldcompare the origin of PPOℓA from the A1 part in thesecases with the POℓA origin in an 18mm human embryowhose picture was displayed in the paper by Katayama etal. [14]. Tsutsumi et al. [8] described that PPOℓA originatedfrom A1-A2 junction. However, many authors described itsinternal carotid origin [7, 9, 14, 16, 19, 21]. In our previouscase the PPOℓA and posterior communicating artery hada common origin from the middle cerebral artery (MCA)[22]. It can be said that the case, described by Lin et al.[21], in which PPOℓA continued from an accessory MCA,resembles our case. Interesting anomaly was found in five ratembryos studied. In these specimens the cranial branch ofthe ICA terminated as the MCA, whereas the POℓA was acontinuation of the primitive maxillary artery [1].

Several types of the PPOℓA are described in the literature.In the first type described by Nozaki et al. [7] the PPOℓArose from the ICA, ran along the olfactory tract, and made ahairpin bend to supply the territory of the ACA postcommu-nicating part (A2). In the second type, described by the sameauthors, the PPOℓA rose from the ACA and passed throughthe cribriform plate of the ethmoid bone to supply the nasalcavity, similar to the ethmoidal arteries.The case described byEnomoto et al. [15], on computer tomography angiography(CTA), and the case described by Moffat [20] on autopsywere classified as the second type. Komiyama [25] noted that

BioMed Research International 3

Right Left

1

23

4

56

78

12910

11

∗

(a)

LeftRight

4

4

5∗

(b)

Figure 1: Persistent primitive olfactory artery (PPOℓA) as a side branch of the precommunicating part (A1) of the right anterior cerebralartery (ACA). It originates at the level of proximal end of the A1 fenestration (a) and courses to the medial surface of the frontal lobe (b).Cerebral part (C4) of the right internal carotid artery (1); left C4 (2); right A1 (3); A1 fenestration (∗); right PPOℓA (4); right recurrent arteryof Heubner (RAH) (5)); anterior communicating artery (ACoA) (6)); left A1 (7); left RAH (8); right postcommunicating part (A2) of the ACA(9); median artery of the corpus callosum (10); left A2 (11); left medial frontoorbital artery (12).

Right Left

12

3

45

6

7

89 11

(a)

LeftRight

3

5

4

4

(b)

Figure 2: Persistent primitive olfactory artery (PPOℓA) as a side branch of the precommunicating part (A1) of the right anterior cerebralartery (ACA). It originates from the anterior wall of the A1 (a) and courses to the medial surface of the frontal lobe, where the PPOℓA gaveoff a bihemispheric branch (b). Cerebral part (C4) of the right internal carotid artery (1); left C4 (2); right A1 (3); right PPOℓA (4); rightrecurrent artery of Heubner (RAH) (5)); anterior communicating artery (ACoA) (6); left A1 (7); left RAH (8); right postcommunicating part(A2) of the ACA (9); left A2 (11).

this second type of the PPOℓA is homologous to the internalethmoidal artery in the dog. In the third (transitory) typedescribed by Horie et al. [13], the PPOℓA divided into twobranches; one artery was similar to Nozaki’s type 1, whereasthe second one had features of Nozaki’s type 2. In our “third”type, the PPOℓA of the MCA origin had a common trunk

with posterior communicating artery (PCoA) and coursedforward to the ipsilateral olfactory tract [22]. The case of thePPOℓA termination (PPOℓA—cortical frontal vein shunt)described by Tsutsumi et al. [8] was classified as type 4.

Medial frontoorbital and frontopolar arteries are differentfrom the PPOℓA according to the beginning (A2 part) and


Table1:Com

paris

onof

generaland

speciald

ataa

bout

thep

ersis

tent

prim

itive

olfactoryartery

(PPOℓA)p

resented

inou

rand

otherinvestig

ations.

Cou

ntry

[autho

rs]

Age∗

Gender(no

.)Initial

symptom

sDiagn

osis

PPOℓA

Incidental

finding

Relatio

nof

number

cases

Vascular

source

Side

Nozaki’s

andnew

types∗∗

Associated

varia

tions

(no.)Aneurysmatic

artery

(no.)

Other

cerebral

patholog

ySinglecases

Korea[

18]

24F

Vertigo

3DCT

A+

ICA

RI

Serbia[22]

35M

Myoc.

infarctio

nAu

topsy

+ICA

pR

III

Orig

in/end

ofther

ight

PCoA

Japan[14

]42

M3D

CTA

+ICA

LI

ACoA

Japan∗∗∗

[15]

44M

Headache

CTA

+(II)

Anasto

m.w

ithleftant.ethm

.a.

Left

fronto-orbital

artery

(PPOℓA)

Intracerebral

hem./S

AH

Japan[7]

54F

Ano

smia

Cereb.

angio.

+ICA

L/R

IAC

oAapl.

RAHsa

pl.

Japan[14

]55

FCereb.

angio.

+ICA

LII

ICA

Japan∗∗∗

[16]

59F

+ICA

LI

ACA

Japan∗∗∗

[17]

59F

Hyposmia

+ICA

RPP

OℓA

Japan[8]

59M

Generalseizure

CTA

+A1-A

2R

(IV)

PPOℓA-

cort.front.

vein

shun

tRA

Hapl.

Intracerebral

hem.

Taiwan∗∗∗

[21]

62F

Cereb.

angio.

+ICA

R(I)

Moyam

oyap

h.Fetal

PCA

MCA

acc.

MCA

occl.

Korea[

19]

68F

Headache

CTA

+ICA

R(I)

PPOℓA

bulbou

sdilatatio

n

Japan[9]

69M

Lossof

consciou

sness

3DCT

A+

ICA

R(I)

ACoA

apl.

PPOℓA/le

ftA1-A

2/ICA

UK[20]

71M

Gastric

carcinom

aAu

topsy

+A1

L(II)

Dou

bleA

CoA

Japan[13]

78M

Headache

Axial

Dyn

aCT/DSA

+A1

RTransitory

type

(I/II

)

PPOℓA-

ethm

oidal

anastomosis

RightA

1SA

H


Table1:Con

tinued.

Cou

ntry

[autho

rs]

Age∗

Gender(no

.)Initial

symptom

sDiagn

osis

PPOℓA

Incidental

finding

Relatio

nof

number

cases

Vascular

source

Side

Nozaki’s

andnew

types∗∗

Associated

varia

tions

(no.)Aneurysmatic

artery

(no.)

Other

cerebral

patholog

yRetro

spectivestudies

Japan[5]

M(1)

Clinica

lor

forensic

investigatio

ns

MRA

1/900

ICA

RJapan[6]

CTA/M

RA1/3

700

ICA

LJapan∗∗∗

[12]

5/?

ICA

PPOℓA(1)

Korea[

11]

24 −82

M(17)

F(12)

MRA

/CTA

29/9841

L(19

)R(7)

LR(3)

ACAhypo

p.(3)

M1fen

(1)

PPOℓA(2)

ICA(1)

Threec

ereb.

arteriæ

(1)

Japan[10]

36 −81

M(6)

F(8)

MRA

14/3491

L(7)

R(6)

LR(1)

VAfen.

(1)

MCA

acc.(1)

MAC

C(1)

MCA

(1)

PPOℓA(1)

Serbia(recentstudy)

0−95

M(2)

Autopsy

2/469

A1

R(2)

IA1fen

(1)

MAC

C(1)

∗

Sing

lecasesa

realignedaccordingto

thea

ge.

∗∗

Nozaki’s[7]a

ndnewtypesa

remarkedby

Romaniannu

mbers.

∗∗∗

Datafrom

thep

aper

byKa

tayamae

tal.[14

].Female(F);m

ale(M);left(L);rig

ht(R);myocardial(myoc.);three-dim

ensio

nalcom

putertom

ograph

yang

iography

(3DCT

A);cerebralangiograph

y(cereb.angio.);digitalsub

tractio

nangiograph

y(DSA

);magnetic

resonancea

ngiography

(MRA

);internalcarotid

artery

(ICA);persistentcranialbranch

oftheinternalcarotidartery

(ICAp );ju

nctio

nofthep

recommun

icatinga

ndpo

stcom

mun

icatingp

arts(A

1-A2)

ofthea

nterior

cerebral

artery

(ACA

);po

sterio

rcommun

icatingartery

(PCoA

);aplasia

oftheanterio

rcommun

icatingartery

(ACoA

apl.);recurrent

artery

ofHeubn

er(RAH);accessorymiddlecerebral

artery

(MCA

acc.);

poste

riorc

erebralartery(PCA

);fenestr

ationof

thes

phenoidpartof

theM

CA(M

1fen);vertebralartery(VA);medianartery

ofthec

orpu

scallosum

(MAC

C);hem

orrhage(

hem.);

occlu

sion(occl.);sub

arachn

oid

hemorrhage(SA

H).


their course. Exceptions were possible as in cases describedby Enomoto et al. [15] and Krishnamoorthy et al. [26].

We described some cases of the POℓA partial persistencein human fetuses [23]. Recently, we described these two casesof the PPOℓA, found only among adult cadavers. Previous[22] and recent cases indicate that the incidence of the PPOℓAis 0.64% in Serbian population. These incidences were 0.14%in the Japanese population [10] and 0.29% in the Koreanpopulation [11]. For the purpose of calculating of number ofpublished cases, we included some paper abstracts [12, 14–17]in the list of references. Based on the case numbers in ourTable 1 and Moffat’s allegation about two cases of the PPOℓAdescribed in 1951 and 1961 by other authors [1], we counted67 cases to this time. Based also on the cases in the sametable, we could note that PPOℓA was more frequent in malesand on the left side, although the POℓA persisted on the rightside in males of Serbian population, as we noted in our work.The existence of bilateral PPOℓA was noted five times in theliterature [7, 10, 11]. The youngest person was 18 years old [5]and the oldest 82 years [11].

In summary, we did not find any aneurysmon the PPOℓAin our cases, opposite to some authors who found it on thePPOℓA hairpin bend [9, 12, 15, 17], and/or on other cerebralarteries [9–11, 13, 14, 16]. Association of the PPOℓA and othervascular variations were also noted [7, 11, 20, 22], as in ouradult cases.

4. Conclusions

The primitive olfactory artery is a rare persistent primitivevessel (0.64%) in Serbian population. It was incidental findingin presented cases. We did not find any complete vasculartrunk in fetuses, but we did in adults of male gender, on theright side.

Acknowledgments

The authors wish to thank Mrs Zorica Antic, Professor ofEnglish in Faculty ofMedicine of Nis, for assistance in editingthe text. Contract Grant sponsor is Ministry of Education,Science and Technological Development of Republic of Ser-bia (nos. 41018 and 175092).

References

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[14] M. Katayama, Y. Shimamoto, and S. Suga, “Primitive olfac-tory artery—characteristics and cerebral aneurysms asso-ciated with primitive olfactory artery,” Niche Neuro-Angi-ology Conference, (Jpn/Eng), 2012, http://nnac.umin.jp/nnac/Download 2012 files/Katayama.pdf.

[15] H. Enomoto, H. Goto, and M. Murase, “A ruptured cerebralaneurysm of the frontoorbital artery and the coexisting anas-tomosis with the anterior ethmoidal artery. A case report,”Neurological Surgery, vol. 14, no. 2, pp. 203–206, 1986.

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[20] D. B. Moffat, “A case of peristence of the primitive olfactoryartery,”Anatomischer Anzeiger, vol. 121, no. 5, pp. 477–479, 1967.

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[26] T. Krishnamoorthy, A. K. Gupta, R. N. Bhattacharya, B. J.Rajesh, and S. Purkayastha, “Anomalous origin of the callo-somarginal artery from the A1 segment with an associatedsaccular aneurysm,” American Journal of Neuroradiology, vol.27, no. 10, pp. 2075–2077, 2006.

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Research Article Persistent Primitive Olfactory Artery in ...primitive olfactory artery (PO A)...

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